Emergence of a Clonal Lineage of Multidrug-Resistant ESBL-Producing Salmonella Infantis Transmitted from Broilers and Broiler Meat to Humans in Italy between 2011 and 2014

Abstract

We report the spread of a clone of multidrug-resistant (MDR), ESBL-producing (bla CTX-M-1) Salmonella enterica subsp. enterica serovar Infantis, in the Italian broiler chicken industry and along the food-chain. This was first detected in Italy in 2011 and led to human infection in Italy in 2013–2014.A set (n = 49) of extended-spectrum cephalosporin (ESC)-resistant (R) isolates of S. Infantis (2011–2014) from humans, food-producing animals and meat thereof, were studied along with a selected set of earlier and more recent ESC-susceptible (ESC-S) isolates (n = 42, 2001–2014). They were characterized by macrorestriction-PFGE analysis and genetic environment of ESC-resistance. Isolates representative of PFGE-patterns and origin were submitted to Whole Genome Sequencing. The emerging ESC-R clone, detected mainly from broiler chickens, broiler meat and humans, showed a minimum pattern of clinical resistance to cefotaxime, tetracycline, sulfonamides, and trimethoprim, beside ciprofloxacin microbiological resistance (MIC 0.25 mg/L). All isolates of this clone harbored a conjugative megaplasmid (~ 280–320 Kb), similar to that described in ESC-susceptible S. Infantis in Israel (pESI-like) in 2014. This megaplasmid carried the ESBL gene bla CTX-M-1, and additional genes [tet(A), sul1, dfrA1 and dfrA14] mediating cefotaxime, tetracycline, sulfonamide, and trimethoprim resistance. It also contained genes conferring enhanced colonization capability, virulence (fimbriae, yersiniabactin), resistance and fitness (qacE1, mer) in the intensive-farming environment. This emerging clone of S. Infantis has been causing infections in humans, most likely through the broiler industry. Since S. Infantis is among major serovars causing human infections in Europe and is an emerging non-typhoidal Salmonella globally, further spread of this lineage in primary productions deserves quick and thorough risk-management strategies.

Comparative Analysis of Extended-Spectrum-β-Lactamase CTX-M-65-Producing Salmonella enterica Serovar Infantis Isolates from Humans, Food Animals, and Retail Chickens in the United States

“…Although antimicrobial treatment is not generally recommended for S. Infantis infections, it is recommended for certain vulnerable hosts or for invasive infections (7). Infections with ESBL-producing organisms are particularly concerning because they are not only resistant to most of the ␤-lactam antimicrobials but also are commonly resistant to additional classes of antimicrobials (8), leaving few treatment options and the potential for worse clinical outcomes. Of the ESBL enzymes, the CTX-M family is the most widely reported in the world, particularly in areas of Europe and Asia (9).…”

“…The emergence of ESBL-producing S. Infantis has been reported in other areas of the world, including Italy and Israel, and this has been connected with the presence of a unique pESI (plasmid for emerging S. Infantis) or pESI-like megaplasmid that enhances the fitness of the bacterium (8,10). Until recently, very few Salmonella isolates with ESBL enzymes or genes had been found in the United States.…”

“…Until recently, the bla CTX-M-65 gene had only been described in a single Escherichia coli isolate from a patient in the United States (11). We used whole-genome sequencing (WGS) to characterize the plasmids from select strains used in this study and to determine the similarity, if any, to the S. Infantis pESI-like megaplasmid previously described by Aviv et al and Franco et al (8,10). We also examined the relatedness of food and human isolates from the United States.…”

Detection of Salmonella Spp. in Feed and Their Antibiotic Susceptibility for Alternative Therapy

“…As presented in table 4, Sal 7 and Sal 8 were resistant to ciprofloxacin due to multi-drug resistant (MDR) gene (Franco et al, 2015). Commonly, minimum inhibitory concentration (MIC) of Salmonella containing MDR was 0.25 µg/mL (Franco et al, 2015).…”

“…Commonly, minimum inhibitory concentration (MIC) of Salmonella containing MDR was 0.25 µg/mL (Franco et al, 2015). The MICs of Sal 7 and Sal 8 were over 1024 µg/mL.…”